Weber, A. W. & Vedder, A. Population dynamics of the Virunga gorillas: 1959–1978. Biol. Conserv. 26, 341–366 (1983).
Google Scholar
Granjon, A.-C. et al. Estimating abundance and growth rates in a wild mountain gorilla population. Anim. Conserv. 23, 455–465 (2020).
Google Scholar
Gray, M. et al. Virunga Massif Mountain Gorilla Census—2010 Summary Report (IGCP & Partners, 2010).
Gray, M. et al. Genetic census reveals increased but uneven growth of a critically endangered mountain gorilla population. Biol. Conserv. 158, 230–238 (2013).
Google Scholar
Robbins, M. M. et al. Extreme conservation leads to recovery of the Virunga mountain gorillas. PLoS One 6, e19788 (2011).
Google Scholar
Hickey, J. R., Granjon, A.-C. & Vigilant, L. Virunga 2015–2016 Surveys: Monitoring Mountain Gorillas, Other Select Mammals, and Illegal Activities (IGCP & Partners, 2019).
Kalpers, J. et al. Gorillas in the crossfire: Population dynamics of the Virunga mountain gorillas over the past three decades. Oryx 37, 326–337 (2003).
Google Scholar
Robbins, M. M., Gray, M., Kagoda, E. & Robbins, A. M. Population dynamics of the Bwindi mountain gorillas. Biol. Conserv. 142, 2886–2895 (2009).
Google Scholar
Hickey, J. R., Uzabaho, E. & Akantorana, M. Bwindi-Sarambwe EM 2018 Surveys: Monitoring Mountain Gorillas, Other Select Mammals, and Human Activities 40 (GVTC, IGCP & Partners, 2019).
Roy, J. et al. Challenges in the use of genetic mark-recapture to estimate the population size of Bwindi mountain gorillas (Gorilla beringei beringei). Biol. Conserv. 180, 249–261 (2014).
Google Scholar
McNeilage, A. J. Mountain Gorillas in the Virunga Volcanoes: Ecology and Carrying Capacity (University of Bristol, 1995).
Caillaud, D., Ndagijimana, F., Giarrusso, A. J., Vecellio, V. & Stoinski, T. S. Mountain gorilla ranging patterns: Influence of group size and group dynamics. Am. J. Primatol. 76, 730–746 (2014).
Google Scholar
Caillaud, D. et al. Violent encounters between social units hinder the growth of a high-density mountain gorilla population. Sci. Adv. 6, eaba0724 (2020).
Google Scholar
Watts, D. P. Causes and consequences of variation in male mountain gorilla life histories and group membership. In Primate Males (ed. Kappeler, P. M.) 169–179 (Cambridge University Press, 2000).
Robbins, M. M., Robbins, A. M., Gerald-Steklis, N. & Steklis, H. D. Socioecological influences on the reproductive success of female mountain gorillas (Gorilla beringei beringei). Behav. Ecol. Sociobiol. 61, 919–931 (2007).
Google Scholar
Robbins, A. M. et al. Impact of male Infanticide on the social structure of mountain gorillas. PLoS One 8, e78256 (2013).
Google Scholar
Grueter, C. C. et al. Quadratic relationships between group size and foraging efficiency in a herbivorous primate. Sci. Rep. 8, 16718 (2018).
Google Scholar
Eckardt, W., Stoinski, T. S., Rosenbaum, S. & Santymire, R. Social and ecological factors alter stress physiology of Virunga mountain gorillas (Gorilla beringei beringei). Ecol. Evol. 9, 5248–5259 (2019).
Google Scholar
Harcourt, A. H., Parks, S. A. & Woodroffe, R. Human density as an influence on species/area relationships: Double jeopardy for small African reserves?. Biodivers. Conserv. 10, 1011–1026 (2001).
Google Scholar
Citterio, C. V. et al. Abomasal nematode community in an alpine chamois (Rupicapra r. rupicapra) population before and after a die-off. J. Parasitol. 92, 918–927 (2006).
Google Scholar
Hudson, P. J. Macroparasites: Observed patterns. Ecol. Infect. Dis. Nat. Popul. 20, 144–176 (1995).
Albon, S. D. et al. The role of parasites in the dynamics of a reindeer population. Proc. R. Soc. Lond. B Biol. Sci. 269, 1625–1632 (2002).
Google Scholar
Anderson, R. M. & May, R. M. Age-related changes in the rate of disease transmission: Implications for the design of vaccination programmes. Epidemiol. Infect. 94, 365–436 (1985).
Google Scholar
Lloyd-Smith, J. O., Schreiber, S. J., Kopp, P. E. & Getz, W. M. Superspreading and the effect of individual variation on disease emergence. Nature 438, 355–359 (2005).
Google Scholar
Anderson, R. M. & May, R. M. Regulation and stability of host-parasite population interactions: I. Regulatory processes. J. Anim. Ecol. 47, 219–247 (1978).
Google Scholar
Arneberg, P., Skorping, A., Grenfell, B. & Read, A. F. Host densities as determinants of abundance in parasite communities. Proc. R. Soc. Lond. B Biol. Sci. 265, 1283–1289 (1998).
Google Scholar
Gillespie, T. R. & Chapman, C. A. Forest fragmentation, the decline of an endangered primate, and changes in host–parasite interactions relative to an unfragmented forest. Am. J. Primatol. 70, 222–230 (2008).
Google Scholar
Mbora, D. N. M. & McPeek, M. A. Host density and human activities mediate increased parasite prevalence and richness in primates threatened by habitat loss and fragmentation. J. Anim. Ecol. 78, 210–218 (2009).
Google Scholar
dos Santos, C. N. et al. Seasonal dynamics of cyathostomin (Nematoda–Cyathostominae) infective larvae in Brachiaria humidicola grass in tropical southeast Brazil. Vet. Parasitol. 180, 274–278 (2011).
Google Scholar
Silangwa, S. M. & Todd, A. C. Vertical migration of trichostrongylid larvae on grasses. J. Parasitol. 50, 278–285 (1964).
Google Scholar
Callinan, A. P. L. & Westcott, J. M. Vertical distribution of trichostrongylid larvae on herbage and in soil. Int. J. Parasitol. 16, 241–244 (1986).
Google Scholar
Crofton, H. D. The ecology of immature phases of trichostrongyle nematodes: II. The effect of climatic factors on the availability of the infective larvae of Trichostrongylus retortaeformis to the host. Parasitology 39, 26–38 (1948).
Google Scholar
Zanet, S. et al. Higher risk of gastrointestinal parasite infection at lower elevation suggests possible constraints in the distributional niche of Alpine marmots. PLoS One 12, e0182477 (2017).
Google Scholar
Derek Scasta, J. Livestock parasite management on high-elevation rangelands: Ecological interactions of climate, habitat, and wildlife. J. Integr. Pest Manag. 6, 20 (2015).
Google Scholar
Huffman, M. A., Gotoh, S., Turner, L. A., Hamai, M. & Yoshida, K. Seasonal trends in intestinal nematode infection and medicinal plant use among chimpanzees in the Mahale Mountains, Tanzania. Primates 38, 111–125 (1997).
Google Scholar
MacIntosh, A. J. J., Hernandez, A. D. & Huffman, M. A. Host age, sex, and reproductive seasonality affect nematode parasitism in wild Japanese macaques. Primates 51, 353–364 (2010).
Google Scholar
Pafčo, B. et al. Do habituation, host traits and seasonality have an impact on protist and helminth infections of wild western lowland gorillas?. Parasitol. Res. 116, 3401–3410 (2017).
Google Scholar
Rothman, J. M., Pell, A. N. & Bowman, D. D. Host-parasiteecology of the helminths in mountain gorillas. J. Parasitol. 94, 834–840 (2008).
Google Scholar
Müller-Graf, C. D. M., Collins, D. A. & Woolhouse, M. E. J. Intestinal parasite burden in five troops of olive baboons (Papio cynocephalus anubis) in Gombe Stream National Park, Tanzania. Parasitology 112, 489–497 (1996).
Google Scholar
Alexander, J. & Stimson, W. H. Sex hormones and the course of parasitic infection. Parasitol. Today 4, 189–193 (1988).
Google Scholar
Bundy, D. A. P. Gender-dependent patterns of infections and disease. Parasitol. Today 4, 186–189 (1988).
Google Scholar
Zuk, M. Reproductive strategies and disease susceptibility: An evolutionary viewpoint. Parasitol. Today 6, 231–233 (1990).
Google Scholar
Nunn, C. & Altizer, S. Infectious Diseases in Primates: Behavior (Ecology and Evolution. Oxford University Press, Oxford, 2006).
Google Scholar
Wilson, K. et al. Heterogeneities in macroparasite infections: Patterns and processes. In The Ecology of Wildlife Diseases 6–44 (2002).
Cattadori, I. M., Boag, B., Bjørnstad, O. N., Cornell, S. J. & Hudson, P. J. Peak shift and epidemiology in a seasonal host–nematode system. Proc. R. Soc. B Biol. Sci. 272, 1163–1169 (2005).
Google Scholar
Terio, K. A. et al. Oesophagostomiasis in non-human primates of Gombe National Park, Tanzania. Am. J. Primatol. 80, e22572 (2018).
Google Scholar
Gillespie, T. R., Nunn, C. L. & Leendertz, F. H. Integrative approaches to the study of primate infectious disease: Implications for biodiversity conservation and global health. Am. J. Phys. Anthropol. 137, 53–69 (2008).
Google Scholar
Collett, M. G. et al. Gastric Ollulanus tricuspis infection identified in captive cheetahs (Acinonyx jubatus) with chronic vomiting: Case report. J. S. Afr. Vet. Assoc. 71, 251–255 (2000).
Google Scholar
Dennis, M. M., Bennett, N. & Ehrhart, E. J. Gastric adenocarcinoma and chronic gastritis in two related Persian cats. Vet. Pathol. 43, 358–362 (2006).
Google Scholar
Smetana, H. F. & Orihel, T. C. Gastric papillomata in Macaca speciosa induced by Nochtia nochti (Nematoda: Trichostrongyloidea). J. Parasitol. 55, 349–351 (1969).
Google Scholar
Nybelin, O. Anoplocephala gorillae n. sp. Ark Zool. 19, 1–3 (1924).
Sleeman, J. M., Meader, L. L., Mudakikwa, A. B., Foster, J. W. & Patton, S. Gastrointestinal parasites of mountain gorillas (Gorilla gorilla beringei) in the Parc National des Volcans, Rwanda. J. Zool. Wildl. Med. 31, 322–328 (2000).
Google Scholar
Ashford, R. W., Lawson, H., Butynski, T. M. & Reid, G. D. F. Patterns of intestinal parasitism in the mountain gorilla Gorilla gorilla in the Bwindi-Impenetrable Forest, Uganda. J. Zool. 239, 507–514 (1996).
Google Scholar
Kalema-Zikusoka, G., Rothman, J. M. & Fox, M. T. Intestinal parasites and bacteria of mountain gorillas (Gorilla beringei beringei) in Bwindi Impenetrable National Park, Uganda. Primates 46, 59–63 (2005).
Google Scholar
Owiunji, I, et al. The biodiversity of the Virunga Volcanoes. https://programs.wcs.org/portals/49/media/file/volcanoes_biodiv_survey.pdf (2005).
Langdale-Brown, I., Osmaston, H. & Wilson, J. G. The Vegetation of Uganda and Its Bearing on Land-Use (Governmentt of Uganda, 1964).
Ashford, R. W., Reid, G. D. F. & Butynski, T. M. The intestinal faunas of man and mountain gorillas in a shared habitat. Ann. Trop. Med. Parasitol. 84, 337–340 (1990).
Google Scholar
Shutt, K. et al. Effects of habituation, research and ecotourism on faecal glucocorticoid metabolites in wild western lowland gorillas: Implications for conservation management. Biol. Conserv. 172, 72–79 (2014).
Google Scholar
Kayiranga, A. et al. Analysis of climate and topography impacts on the spatial distribution of vegetation in the Virunga Volcanoes Massif of East-Central Africa. Geosciences 7, 17 (2017).
Google Scholar
Cousins, D. & Huffman, M. A. Medicinal properties in the diet of gorillas: An ethno-phramacological evaluation. Afr. Stud. Monogr. 23, 65–89 (2002).
Woolhouse, M. E. J. Patterns in parasite epidemiology: The peak shift. Parasitol. Today 14, 428–434 (1998).
Google Scholar
Hayes, K. S., Bancroft, A. J. & Grencis, R. K. Immune-mediated regulation of chronic intestinal nematode infection. Immunol. Rev. 201, 75–88 (2004).
Google Scholar
Maizels, R. M. et al. Helminth parasites—masters of regulation. Immunol. Rev. 201, 89–116 (2004).
Google Scholar
Proudman, C. J., Holmes, M. A., Sheoran, A. S., Edwards, S. E. R. & Trees, A. J. Immunoepidemiology of the equine tapeworm Anoplocephala perfoliata: Age-intensity profile and age-dependency of antibody subtype responses. Parasitology 114, 89–94 (1997).
Google Scholar
Gergócs, V., Garamvölgyi, Á., Homoródi, R. & Hufnagel, L. Seasonal change of oribatid mite communities (Acari, Oribatida) in three different types of microhabitats in an oak forest. Appl. Ecol. Environ. Res. 9, 181–195 (2011).
Google Scholar
Dobson, A. & Foufopoulos, J. Emerging infectious pathogens of wildlife. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 356, 1001–1012 (2001).
Google Scholar
Xue, Y. et al. Mountain gorilla genomes reveal the impact of long-term population decline and inbreeding. Science 348, 242–245 (2015).
Google Scholar
Reed, D. H. & Frankham, R. Correlation between fitness and genetic diversity. Conserv. Biol. 17, 230–237 (2003).
Google Scholar
Pafčo, B. et al. Metabarcoding analysis of strongylid nematode diversity in two sympatric primate species. Sci. Rep. 8, 5933 (2018).
Google Scholar
McNeilage, A. Diet and habitat use of two mountain gorilla groups in contrasting habitats in the Virunga. In Mountain Gorillas: Three Decades of Research at Karisoke (Cambridge University Press, 2001).
Sinayitutse, E. et al. Daily defecation outputs of mountain gorillas (Gorilla beringei beringei) in the Volcanoes National Park, Rwanda. Primates https://doi.org/10.1007/s10329-020-00874-7 (2020).
Google Scholar
Burgunder, J. et al. Complexity in behavioural organization and strongylid infection among wild chimpanzees. Anim. Behav. 129, 257–268 (2017).
Google Scholar
Chapman, C. A., Speirs, M. L., Gillespie, T. R., Holland, T. & Austad, K. M. Life on the edge: Gastrointestinal parasites from the forest edge and interior primate groups. Am. J. Primatol. 68, 397–409 (2006).
Google Scholar
Anderson, R. M. & Schad, G. A. Hookworm burdens and faecal egg counts: An analysis of the biological basis of variation. Trans. R. Soc. Trop. Med. Hyg. 79, 812–825 (1985).
Google Scholar
Warnick, L. D. Daily variability of equine fecal strongyle egg counts. Cornell Vet. 82, 453–463 (1992).
Google Scholar
Tomczuk, K. et al. Comparison of the sensitivity of coprological methods in detecting Anoplocephala perfoliata invasions. Parasitol. Res. 113, 2401–2406 (2014).
Google Scholar
Williamson, R., Beveridge, I. & Gasser, R. Coprological methods for the diagnosis of Anoplocephala perfoliata infection of the horse. Aust. Vet. J. 76, 618–621 (1998).
Google Scholar
Cringoli, G. et al. The Mini-FLOTAC technique for the diagnosis of helminth and protozoan infections in humans and animals. Nat. Protoc. 12, 1723–1732 (2017).
Google Scholar
Guschanski, K. et al. Counting elusive animals: Comparing field and genetic census of the entire mountain gorilla population of Bwindi Impenetrable National Park, Uganda. Biol. Conserv. 142, 290–300 (2009).
Google Scholar
Zuur, A., Ieno, E. N., Walker, N., Saveliev, A. A. & Smith, G. M. Mixed Effects Models and Extensions in Ecology with R (Springer, 2009).
Google Scholar
Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).
Google Scholar
R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ (2020).
Forstmeier, W. & Schielzeth, H. Cryptic multiple hypotheses testing in linear models: Overestimated effect sizes and the winner’s curse. Behav. Ecol. Sociobiol. 65, 47–55 (2011).
Google Scholar
Engqvist, L. The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies. Anim. Behav. 70, 20 (2005).
Google Scholar
Gelman, A. & Hill, J. Data Analysis Using Regression and Multilevel/Hierarchical Models (Cambridge University Press, 2007).
Schielzeth, H. Simple means to improve the interpretability of regression coefficients. Methods Ecol. Evol. 1, 103–113 (2010).
Google Scholar
Johnson, J. B. & Omland, K. S. Model selection in ecology and evolution. Trends Ecol. Evol. 19, 101–108 (2004).
Google Scholar
Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach (Springer, 2002).
Google Scholar
Barton, K. MuMIn: Multi-Model Inference. R package version 1.43.17. https://CRAN.R-project.org/package=MuMIn (2020).
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